Permeability of habitat edges for Ringlet butterflies (Lepidoptera, Nymphalidae, Erebia Dalman 1816) in an alpine landscape

Nota Lepi. 43 2020: 29-41 | DOI 10.3897/n1.43.37762 Research Article

Permeability of habitat edges for Ringlet butterflies (Lepidoptera,
Nymphalidae, Erebia Dalman 1816) in an alpine landscape

ANDREA GRILL!, DANIELA POLIC?, ELIA GUARIENTO?, KONRAD FIEDLER*

1 Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland

2 Department of Biology and Environmental Science, Linnaeus University, Hus Vita, SWE-44050, Kalmar, Sweden
3 Institute for Alpine Environment, Eurac Research, Viale Druso 1, IT-39100 Bolzano / Bozen, Italy

4 Department of Botany and Biodiversity Research, University of Vienna, Rennweg 14, A-1030 Wien, Austria

http://zoobank. org/FEB59D1E-DC09-4A 9F-9117-B3BE8EC405C1

Received 28 June 2019; accepted 27 November 2019; published: 14 February 2020
Subject Editor: Martin Wiemers.

Abstract. We tracked the movements of adult Ringlet butterflies (Lepidoptera, Nymphalidae, Erebia Dalman,
1816) in high-elevation (> 1800 meters a.s.l.) grasslands in the Austrian Alps in order to test if an anthropogenic
boundary (= an asphalt road) had a stronger effect on butterfly movement than natural habitat boundaries (trees,
scree, or dwarf shrubs surrounding grassland sites). 373 individuals (136 females, 237 males) belonging to 11
Erebia species were observed in one flight season (July-August 2013) while approaching or crossing habitat
edges. Erebia pandrose (Borkhausen, 1788) was the most abundant species with 239 observations. All species
studied were reluctant to cross habitat boundaries, but permeability was further strongly affected by the border
type. Additional variables influencing movement probability were species identity and the time of the day. In E.
pandrose, for which we had sufficient observations to analyse this, individuals were more likely to cross a bound-
ary in the morning and in the late afternoon than at midday. Erebia euryale (Esper, 1805) and E. nivalis Lorkovi¢
& de Lesse, 1954 were more likely to leave a habitat patch than their studied congeners. The key result of our
study is that the paved road had the lowest permeability among all edge types (0.1 likelihood of crossing when
approaching the edge). A road cutting across a conservation area (viz. a national park) thus hinders inter-patch ex-
change among Ringlet butterflies in the alpine zone, even though theoretically they ought to be able to fly across.

Introduction

An “edge” can be defined as any boundary between two ecosystems inhabited by different biologi-
cal communities or as “transitional zones between adjoining ecosystems or habitats” (e.g., Magura
et al. 2017 and references therein). In alpine landscapes, which are the focus of this study, natural
edges exist, for instance, where grasslands border scree, shrubs, or woodland. Alternatively, there
are anthropogenic edges, like roads crossing a habitat or the borders to areas under different modes
of land-use. Most anthropogenic edges are characterized by sharper environmental contrasts and
have been described to be less permeable than natural ones in a number of studies (e.g., Ascensao
et al. 2017 for mammals; Magura et al. 2017 for beetles; Baguette and Van Dyck 2007 for insects;
Ries and Debinski 2001 and Polic et al. 2014 for butterflies). Permeability is a term coined by
movement ecologists and usually defined as “the degree to which a barrier inhibits movement”
(Beyer et al. 2016); where a barrier is a feature in the landscape that can be “crossed but not
circumnavigated”. Various animal groups living in vegetated habitats, such as small mammals
(Ascensao et al. 2017), amphibians (Matos et al. 2017) and elephants (Wadey et al. 2018) have

30 ANDREA GRILL ef al.: Behaviour of Erebia butterflies at habitat edges

been reported to avoid areas lacking vegetation cover. It has been suggested that this avoidance
behaviour is innate to terrestrial organisms living in vegetated habitats. Consequently, depending
on species-specific responses vegetation-free elements may even act as complete barriers for ani-
mals when moving through the landscape (Beyer et al. 2016). Among the most impermeable edges
are asphalted linear infrastructures ubiquitous worldwide: roads (Forman et al. 2003; van der Ree
et al. 2015). In winged animals, data on how movement behaviour 1s affected by roads have so far
been collected mainly for birds (Lima et al. 2015; Rytwinski and Fahrig 2015) which clearly react
to roads and were even found to adjust their flight behaviour to speed limits of traffic on roads
(Legagneux and Ducatez 2013), and to reduce the amount of parental care given to fledgelings
(e.g., Ng et al. 2019) when living next to a road. In insects, such data are even more limited, espe-
cially for habitats outside the usual European lowlands under more or less intense agricultural use
(Mufioz et al. 2015; Jacobson et al. 2016; Andersson et al. 2017). Together with a previous study
in 2012 (Polic et al. 2014) we were the first to attempt to obtain data on the effect of a road on the
movement of Erebia Dalman, 1816 butterflies in high elevation grasslands.

Whereas our first study was a mark-release-recapture experiment, we now focused on tracking the
movement of individual un-manipulated adult butterflies at four edge types bordering their natural
grassland habitats: (a) trees, (b) scree, (c) dwarf shrubs, (d) roads. Eleven Evebia species that we knew
to be present in the area were chosen as target species for observation (see Table 1 for list of species).

We hypothesized that the anthropogenic boundary (1.e., the asphalt road) would have a lower
permeability than the natural boundaries and that this effect would be similar for all studied species
in this butterfly genus. We also tested if the time of the day affected the likelihood of crossing a bor-
der as it has been suggested that temporal changes 1n activity may be important in explaining edge
responses in butterflies (Siu et al. 2016). This could be important if traffic (ca. 270,000 vehicles per
year between May and November, GroBglockner HochalpenstraBen AG pers. comm., 2013) were
to be limited for nature management purposes.

Material and methods
Study area

This study was carried out in the Hohe Tauern National Park in Austria, in grassland habitats located
at elevations of 1,850 to 2,400 ma.s.l. from 12.vii.2013 to 12.vi1.2013. The Hohe Tauern National
Park comprises many habitats important to Ringlet butterflies, such as different types of grassland
and dwarf shrub heaths, and 21 Evebia species are known to occur within its boundaries (Huemer
and Wieser 2008). We selected 8 study plots on grassland sites on the north facing side of the national
park which is situated in the province of Salzburg (see Figure 1), coordinates of the sites in longi-
tude/latitude were as follows: A = 47.1220°N/12.8240°E, B = 47.1213°N /12.8237°E, C =47.1188°N
/12.8269°E, D = 47.1202°N /12.8242°E, E = 47.1300°N /12.8065°E, F = 47.1284°N /12.8050°E, G
= 47.1296°N /12.8060°E, H = 47.1258°N/12.8083°E. These plots were of similar physical structure
and relatively homogeneous with respect to slope and nectar resources with only small parts of open
soil and rocks interspersed but differed in the habitat boundaries to which they were adjacent. They
ranged from 20 to 100 metres in length and 10 to 100 metres in width, depending on the local con-
ditions. Each plot bordered one of the four boundary types on one side and grassland on the other
side, so that each boundary type was replicated once. The four boundary types are: shrubs (=dwarf
shrub heaths, mostly comprising species of Rhododendron L., Vaccinium L. and Juniperus L.), scree

Nota Lepi. 43: 29-41 31

Sources: Esri, DeLorme, HERE, MapmylIndia, DigitalGlobe, GeoEye, i-cubed, USDA FSA, USGS,
AEX, Getmapping, Aerogrid, IGN, IGP, swisstopo, and the GIS User Community

Figure 1. Map of the study site with the locations where butterflies were observed.

(= barely vegetated stony areas), trees (= isolated stands in the generally low vegetated landscape,
usually spruce Picea abies (L.) H. Karst. in the region), and the asphalt road (= a large road of an
average width of 8 m) cutting across the national park. The road was built in 1935 and is intensive-
ly used by motorized traffic during the summer season. All plots were inhabited by Evebia adults
(which we had verified by observations the previous year). These were observed across the whole
of each respective plot.

Study system: Erebia butterflies

Ringlets are univoltine or semivoltine species with adults flying from May to September, depending
on species and altitude. The larvae feed on grasses or sedges, and in many alpine species the de-
velopment takes two years (Sonderegger 2005). Often several Erebia species occur sympatrically,
which is why we chose them for this study. Possible differences in reaction to edge type are unlikely
to result from phylogenetic origin, as the morphology and physiology of these butterflies are, apart
from body size and minor differences in wing patterns, very much alike. This makes the genus an
excellent system for studying edge permeability across multiple species in an alpine landscape.

Behavioural data

To analyse a butterfly’s response to habitat edges, we used a variation of the point-release approach
(e.g., Schultz et al. 2012; Kallioniemi et al. 2013). We checked plots across the whole width and length
for butterflies engaging in flight towards a bordering structure. As soon as a butterfly moved towards

32 ANDREA GRILL ef al.: Behaviour of Erebia butterflies at habitat edges

a bordering structure, we recorded its behaviour. If there were still butterflies on a site that did not en-
gage in flight towards a boundary after that, we did not include these individuals and moved on to the
next site. Only spontaneously flying individuals were chosen for observation. Butterflies that nectared
at the time we discovered them were not included in the analysis, as the intake of nectar might have
influenced their subsequent behaviour. Then we recorded if the butterfly crossed the border or not,
assigning a score of 1 or 0, respectively. After observing the edge-mediated behaviour of a butterfly,
it was caught with a hand-held net and species identity and sex were determined. Age was estimated
by wing-wear on a rank scale (1 = fresh, 2 = wings slightly fringed, 3 = pieces of wing missing, 4 =
highly damaged wings; this is a commonly used approach to estimate butterfly age, e.g. Walters et al.
2012). Butterflies were released immediately after handling at the point of capture, viz. on either side
of the respective boundary. Thus, only an individual’s complete crossing behaviour was assigned to a
score of 1, and a score of 0 was assigned if it engaged in a u-turn and stayed on the site; an individual
that entered the boundary but did not cross was also classified as 0. In this way, the butterfly’s flight
remained natural and un-manipulated during the behavioural decision. Dispersing butterflies coming
from outside and leaving the respective site were not included tn the analysis. For every butterfly, we
noted date and time of capture. All observations were carried out by the same observer. Depending on
the weather conditions and thus the butterflies’ activity, each site was visited daily (in total between 4
and 12 visits per site) and the observation time per visit ranged from 30 minutes up to 1 hour per site.
Observations were carried out between 9:00 and 17:00, according to the butterflies’ activity. Observa-
tions only took place during fair weather conditions, 1.e. during sunny to partly cloudy weather when
butterflies were active. A few observations (N < 5) that occurred during periods of strong winds, which
might have caused accidental dispersal of individuals, were not included in the analyses.

Statistical analyses

For statistical analyses, the incidences of the crossing (1) vs. the avoidance of boundaries (0) were
used. Generalised linear mixed models (GLMM) with binomial error structure were implemented
for analysing the likelihood of crossing between the different boundary types (modelled as fixed
factors). Species affiliation was included as random factor to take into account the potential be-
havioural differences between the species involved. The analyses were performed in the R environ-
ment (R Core Team 2017) using the package Ime4 (Bates et al. 2015). Explained variance through
fixed effects, as well as fixed plus random effects, were expressed as marginal and conditional R?
values. Further, generalised linear models (GLM), also with binomial error structure, were used to
analyse possible differences between species. For Erebia pandrose (Borkhausen, 1788), for which
we had substantially more observations than for all other species, the likelihood of crossing was
further analysed with GLMs regarding the time of the day (categorical fixed factor with morning
defined as the time between 9:00 and 11:00, midday between 11:00 to 15:00 and afternoon after
15:00) and the potential differences between the two un-vegetated border types, road and scree.
Graphical representations of the results were obtained using the package ggplot2 (Wickham 2009).

Results

Edge permeability

We captured 373 individuals (136F, 237M) belonging to 11 Erebia species (see Table 1), among
which the largest proportion of individuals (239) belonged to EF. pandrose. The number of observed

Nota Lepi. 43: 29-41 33

Table 1. Individuals observed per Erebia species (f = female, m = male), only individuals with more than 10
observations were used for further analyses.

Species f m Captures Sex-ratio
E. aethiops 2 1 3 Bs
E. epiphron 5) 25 30 0.2
E. eriphyle 7 Ps 14 1
E. euryale 6 21 27 0.3
E. gorge 3 6 9 0.5
E. ligea 2 3 5 0.7
E. manto 4 0 4
E. melampus 1 + 5 (53
E. nivalis 4 10 14 0.4
E. pandrose 98 141 209 0.7
E. pharte 4 19 23 0.2
Total 136 237 373
0.6

D

e

7)

a

es 0.4

Ke)

se)

12)

o

x=

o

x

wal O72

Road Trees Scree Shrubs
Borders

Figure 2. Permeability at four different edge types (road, scree trees, shrubs) for Erebia adults depicted as the
proportion of individuals approaching an edge and crossing it, a likelihood of 0.1 means that 10% of individ-
uals are likely to cross. Whiskers represent the confidence interval.

crossings was significantly different across edge types (Figure 2; Likelihood-ratio of fixed factor
border-type: Chr’= 9.569; p= 0.02; Runa te ditional = 0-08 / 0.50). Permeability was lowest at the
edge-type “road” for all species (Z= -2.25, p = 0.02), with a likelihood of crossing of less than 0.1,
followed by “trees” and “scree” (<0.4). “Shrubs” was most permeable for all studied species, but
also here the likelihood of crossing scored below 0.5.

The total number of crossings differed significantly between species (Figure 3; Chi? = 77.31;
p < 0.001; R*= 0.19). Among the species for which we had more than 10 observations, E. euryale

(Esper, 1805) was most likely to cross a habitat edge (> 0.5), followed by E. nivalis Lorkovi¢ & de

34 ANDREA GRILL ef al.: Behaviour of Erebia butterflies at habitat edges

Lesse, 1954. E. eriphyle (Freyer 1836), E. pandrose, E. pharte (Hubner, 1803—1804) and E. epiphron
(Knoch, 1783) were all similarly reluctant to cross an edge (< 0.25) (see Figure 3). Testing the per-
meability of “scree” versus “road” (both represent un-vegetated areas; Chi? = 9.82; p = 0.002; R?=
0.05) for E. pandrose, for which we had a sufficient number of observations to make a comparison,
showed that the road was significantly less permeable (Figure 4; GLM: Z = -6.98; p < 0.001) than
“scree” (GLM: Z = 2.96; p = 0.003). Gender and age did not noticeably affect crossing behaviour.

0.75]
>
Cc
7)
n
e
© 0.504
e— =
fe)
se}
fe)
fe)
—
2 0.25]
a

0.00} |

euryale nivalis eriphyle pandrose pharte epiphron
Species

Figure 3. Likelihood of crossing any habitat edge when approaching it for six different Erebia species: eu-
ryale, nivalis, eriphyle, pandrose, pharte, epiphron, a likelihood of 0.1 means that 10% of individuals are
likely to cross. Whiskers represent the confidence interval.

0.3
= @
Oo
3
5 0.2
re)
OD =|)
|
|
&
@
x
=

0.1

Road Scree

Borders
Figure 4. Permeability of an anthropogenic (road) versus a natural (scree) unvegetated habitat edge for Erebia

pandrose adults, depicted as the proportion of individuals approaching and crossing it, a likelihood of 0.1
means that 10% of individuals are likely to cross. Whiskers represent the confidence interval.

Nota Lepi. 43: 29-41 a5

Time-of-day effects

The time of day significantly affected the likelihood of crossing for E. pandrose individuals (GLM:
Chi? = 14.269; p < 0.001; R?= 0.07). In the mornings (9:30—11:00; Z = 0.65; p = 0.516) and in the
afternoon (after 15:00; Z=-4.75; p < 0.001) butterflies were more inclined to move across an edge
than in the middle of the day (11:00—15:00; Z = -2.84; p = 0.004) (Figure 5). Using the whole data
set (11 species) or only the smaller sized grassland species (E. pharte, melampus (Fuessly, 1775),
epiphron, manto (Denis & Schiffermiuller, 1775)), this pattern disappeared (Table 2). Generally,
observations after 15:00 concerned mainly E. pandrose, the other Ringlet species had mostly al-
ready retreated to rest by that time.

Likelihood of crossing

2°
—

oO
‘s)

Morning Midday Early afternoon Afternoon

Figure 5. Likelihood of crossing a habitat edge when approaching it for the species Erebia pandrose in re-
lation to the time of the day, a likelihood of 0.1 means that 10% of individuals are likely to cross. Whiskers
represent the confidence interval.

Table 2. Edge permeability for Erebia butterflies as the proportion of individuals approaching an edge that
cross in relation to time of day.

Cross 1170] Sum
only Erebia pandrose 0 199
1 40
Sum 239
Prob(cross) 0.17
smaller sized Erebia-species 0 65
(pharte, melampus, eriphyle, 1 11
epiphron, manto) Sum 76
Prob(cross) 0.14
All Erebia-species 0 286
1 87
Sum 373
Prob(cross) 0.23

36 ANDREA GRILL ef al.: Behaviour of Erebia butterflies at habitat edges

Discussion

Road and species effects

Our results support the hypothesis that the road has a far lower permeability for Erebia butterflies
than naturally un-vegetated areas (screes, in our study); this effect was consistent across all studied
Ringlet species and also consistent with our earlier findings (Polic et al. 2014). The road, however,
was not a complete barrier since a few individuals of the species E. pandrose (10 individuals),
nivalis (1) and epiphron (1) did cross (Table 3). Generally, all studied species avoided crossing
habitat boundaries, natural and anthropogenic ones, similar to findings in other studies on the be-
haviour of butterflies at habitat edges (Polic et al. 2014; Mair et al. 2015).

Another key result from our study was that the likelihood of crossing habitat boundaries dif-
fered between species within the genus Erebia: E. euryale and E. nivalis were clearly more likely
to leave a habitat patch than the other species. Erebia nivalis has been suggested to be a relatively
good disperser in a mark-release-recapture study performed in the same year and in the same
area as our study (Ehl et al. 2016), with a potential dispersal distance calculated to be up to five
kilometres. Most individuals, however, are reported to be rather sedentary, similar to our findings.
Those authors also reported that females of FE. nivalis are less active fliers than males but are the
ones more likely to undertake long-distance flights. In former mark-release-recapture work that
compared the movement of six different Evebia species (eriphyle, epiphron, pharte, gorge (Hub-
ner, 1803-1804), pandrose, nivalis) we found only E. pharte to be more likely to change between
plots than the other Ringlet species (Polic et al. 2014). It is important to note that Erebia butterflies
are generally rather sedentary, more than half of the individuals marked in this earlier experiment
(Polic et al. 2014) did not move more than 25 metres between recapture events.

With regard to behavioural responses of other genera of butterflies at habitat boundaries, Mair et al.
(2015) did not find differences between the likelihood of crossing for the three lycaenid species, Poly-
ommatus icarus (Rottemburg, 1775), Aricia agestis (Denis & Schiffermuller, 1775) and Plebejus argus
(Linnaeus, 1758). In their study, they observed behavioural responses that varied from ‘soft’? bounda-
ries (= broadly similar vegetation structure) to ‘hard’ boundaries (= tall trees with few nectar sources).
They found that activity levels within the habitat differed among the three species and concluded that
the most active species in general are also the most likely to cross habitat boundaries. In our study, we
cannot differentiate between activity and abundance, as we only observed the individuals that were
actually moving and did not attempt to collect abundance measurements. Nevertheless, E. pandrose
was obviously the most abundant species, but not the most likely to cross boundaries (see Figure 3).

In our data, edge type was decisive for the likelihood of crossing. When looking at the individual
movements of FE. euryale and E. nivalis (Table 3), we found that for the former species all movements
across edges were directed towards trees or shrubs and for the latter species all crossing movements
occurred towards scree or the road. This can be explained by the species’ ecology and habitat prefer-
ences: E. euryale is a montane species that lives in a variety of habitats. It inhabits open mountain for-
ests from above 800 m up towards the tree-line, and 1s often associated with spruce forest clearings,
but it can also occur in more exposed slopes and subalpine meadows. Therefore, trees or shrubs do
not represent boundaries for E. euryale. The association with open woodland is most likely the reason
for its readiness to cross the edge towards higher vegetation like trees and shrubs, an inclination that
the other studied species entirely lacked. On the other hand, Erebia nivalis, a Ringlet species endemic
to the eastern central Alps, is restricted to elevations above 1800 m, typically above the treeline, and

Nota Lepi. 43: 29-41 37

Table 3. Individual crossing behaviour per species (t = crossed; M = stayed on patch).

E. pandrose t NM total E. epiphron + N total E. euryale ik NM total
n(ind) n(ind) n(ind)

scree 30 =—87 scree 2 6 scree 0 0

road 10 109 road 1 20 road 0) 0)

trees 0 2 trees 0 0 trees Wong 07,

shrubs 0 1 shrubs 1 0 shrubs a 1

total (observations) 40 199 239 4 26 30 19 8 27

E. pharte tT a E. eriphyle + a E. nivalis t a

scree 0 0 scree 0 1 scree 4 5

road 0 0 road 0 2 road 1 4

trees 1 9 trees 0 6 trees 0 0

shrubs 2 11 shrubs 3 2 shrubs 0 0

total (observations) 3 20 23 3 1] 14 5 9 14

E. gorge ‘i N E. ligea tT a E. melampus + a

scree 9 0 scree 0 0 scree 0 0

road 0 0 road 0 0 road 0 0

trees 0 0 trees 0 5 trees 0 3

shrubs 0 0 shrubs 0 0 shrubs 1 1

total (observations) 9 0 9 0 5 5 1 4 5

E. manto ‘i N E. aethiops ¢ a

scree 0 0 scree 0 0

road 0) 0 road 0 0

trees 0 1 trees 0 0

shrubs 0 3 shrubs 3 0

total (observations) 0 4 4 3 0 3

occurs on barely vegetated sunny, rocky and often steep slopes with only patches of vegetation (Son-
deregger 2005). It actively seeks barren areas for thermoregulation (R. Verovnik, pers. comm., 2019),
and so scree and even the road constitute less of a barrier for this species than vegetated areas, like
dwarf shrubs and trees. Thus, species that also live in the montane and subalpine zone, where forest
is part of the natural habitat (£. euryale, pharte), are more inclined to fly across habitat borders com-
prising higher vegetation like trees or shrubs than species truly restricted to alpine areas (E. nivalis).

The fact that E. pandrose and E. epiphron were the most frequently sighted butterflies in our
study is not too surprising per se. They are often reported to be the most abundant Ringlet species
above the timberline (e.g., Cizek et al. 2003) and E. epiphron was also quite abundant in the pre-
vious year (Polic et al. 2014). It is surprising, however, that in the year before individuals of E.
pandrose were among the least captured in the mark-release-recapture study (Polic et al. 2014) and
only 34 individuals were marked during the entire season (between 7.vii. and 12.viii.). So it seems
that 2013 was a particularly good year for E. pandrose.

The general avoidance of the asphalt road could be related to the lack of complex ground cover,
which 1s perceived by the butterflies. Although we have no data on a butterfly’s view of anthropo-
genic infrastructural objects, we presuppose that large asphalted areas offer no place to hide, and are
avoided by butterflies as crossing them would increase their predation risk. Besides, they are obvi-
ously also a resource free zone, 1.e. a non-habitat. In the natural boundaries we studied there may be
the occasional nectar source. As we know from earlier work (Polic et al. 2014) the presence of nectar
sources affects movement behaviour of Erebia butterflies. We did not study the impact of traffic
intensity on the permeability of the road, but following our field observations it seems likely that the
sheer presence of asphalted ground hinders butterfly movement, and not the approaching vehicles.

38 ANDREA GRILL ef al/.: Behaviour of Erebia butterflies at habitat edges

Time effects
The likelihood of E. pandrose adults crossing a habitat edge peaked in the mornings and afternoons
whereas it was much lower in the middle of the day. This behaviour probably reflects the daily activity
patterns of the species. Other authors have also observed clear diurnal patterns in the behaviour of Er-
ebia species (E. epiphron and E. euryale) in alpine grasslands in the Eastern Sudetes (Konvitka et al.
2002) where they found that males were more active fliers than females and bask in the mornings, then
patrol for mate-location as soon as it gets warmer with an activity peak just before noon and nectar in the
afternoons, while mated females oviposit in the afternoons. This diurnal pattern seems to be characteris-
tic for mountain Erebia adults (Konvicka et al. 2002), as low temperatures seem to be the limiting factor
for butterflies’ activity in mountain and alpine habitats and the butterflies utilize each sunny moment for
nectaring and mate location. For a lowland representative of the genus, like E. aethiops (Esper, 1777),
however, high temperatures seemed to limit their flight activity (Slamova et al. 2010). This species was
observed to spend the hottest part of the day in the shade, similar to our observations of E. pandrose.

Similar diurnal activity alterations were also observed for a number of other nymphalid butter-
flies (Grill 2003; Peixoto and Benson 2009), and are often related to an avoidance of stressful ther-
mal conditions and to increase the chance to mate. In the case of two sympatric tropical satyrine
butterflies (Peixoto and Benson 2009), one species showed a similar diurnal activity pattern to E.
pandrose, with peaks in the morning and afternoon. In the other species, however, flight activity
peaked at mid-day, probably due to their territorial behaviour. If territorial behaviour plays a role
at all among the studied Erebia species, this was not evident in the field situation and could not
be observed or quantified. Considering that Erebia species are generally cold-adapted (Slamova et
al. 2010), and as solar radiation can be very strong on the slopes where our study was carried out,
also the dark coloured E. pandrose may choose to rest during the hours of the day when the sun
approaches its zenith in order to avoid overheating.

With the knowledge that crossing probability may change during the day, a time-frame (for example
the morning hours) could be envisaged for limiting (or banning) traffic and providing temporal win-
dows for butterflies to facilitate their crossing of the road during the hours when they are most active.

Conclusions

The most important finding of this study is that the road indeed represents the strongest barrier to
the movement of Evebia butterflies among the studied habitat edges. Reluctance of Erebia butter-
flies to cross the road is probably related to the different texture of the road, not to the intensity
of traffic (A. Grill, pers. observation). The road definitely reduces inter-patch exchange of Erebia
butterflies in a large Austrian nature reserve.

Roads are thus not only affecting the home ranges of large animals, for which they are well known
to alter landscape permeability (e.g., Wadey et al. 2018), but also for small flying insects, like butter-
flies, for which this may not be as obvious. Strategies to make roads more permeable have up to now
mainly been implemented for vertebrates. Temporal closures, for example, have been shown to be
beneficial for mammals in a Canadian national park (Whittington et al. 2019), and the installation of
vegetated bridges has been highly beneficial for forest microbat communities in Australia (McGre-
gor et al. 2017). In this case, the vegetated overpasses facilitate habitat continuity across a four-lane
road separating two forest reserves near Brisbane for a wide range of species from small flying
vertebrates to reptiles and amphibians. Similar structures would surely also enhance connectivity of
habitats across asphalt roads for butterflies or other insects in the Hohe Tauern National Park.

Nota Lepi. 43: 29-41 39

Notably, our data suggest that for some Ringlet species the barrier effect of the road 1s more pro-
nounced than for others. Species with high phenotypical similarity may behave quite distinctly when
approaching habitat boundaries. Seeking a deeper understanding of the diversity of Ringlet butter-
flies along behavioural and ecological gradients seems therefore worthwhile, for example with regard
to the fate of these emblematic alpine insects in response to ongoing climate and land-use change.

Acknowledgements

This work was supported by an Austrian Science Foundation (FWF) grant to Andrea Grill
(V169-B17) and funds from the University of Vienna. Permits for handling Erebia butterflies were
obtained from the regional government of Salzburg. We also thank five reviewers for their critical
comments on the manuscript, which helped us to improve its clarity and style.

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